PhD School in Psychology Department of Cognitive Science Budapest University of Technology and Economics

(1)

1

PhD School in Psychology Department of Cognitive Science

Budapest University of Technology and Economics

The ERP Correlates of the Prosodic Processing in Preterm and Full-term Infants

Thesis booklet

Zsuzsanna Sólyom-Varga

Supervisor: Prof. Dr. Valéria Csépe

Budapest, 2021

(2)

2 Introduction

This dissertation aims to explore the prosodic processing of full-term (FT) and preterm (PT) infants in the first year of life. In this sensitive period of language acquisition, event-related brain potential (ERP) correlates of word stress processing are discussed from two different aspects. Firstly, we compared the PT and FT infants’ mismatch negativity components, elicited by word stress discrimination. We discussed the development of the PT infants’

prosodic processing according to the “Delayed versus Disrupted” proposal. Secondly, we investigated how stress cue and lexical status interact in typically developing Hungarian FT infants acquiring a fixed stress language.

The unanimous conclusion of developmental psychological and psycholinguistic research is that preterm (PT) birth enhances the risk of atypical language development (Barre et al. 2011; Pritchard et al. 2014; Sansavini et al. 2010). In the present dissertation, I review studies related to PT infants’ language development before school age, and I discuss those sampling issues that impede the thorough exploration of PT infants’ language development.

Previous studies have indicated that atypical language development has precursors in infants’

event-related potential (ERP) correlates of word stress processing (Friedrich et al. 2009;

Ference et al. 2013). Only a few studies to date have examined PT infants’ early auditory processing, and these have focused mainly on the neonatal period (Bisiacchi et al. 2009;

Mento et al. 2010). By contrast, studies that have examined the development of PT infants’

early linguistic processing (at 3–12 months) have not considered the possible effect of neonatal risk factors like gestational age and birth weight (Peña et al., 2010, 2012; Ragó et al., 2014).

A further unanswered question is related to PT infants’ maturation—that is, whether their prosodic processing is delayed or disrupted (Gervain, 2018). Determining whether PT infants’ prosodic development is disrupted or delayed would not only contribute to the

(3)

3

development of intervention programs for neonatal intensive care units (NICUs) but would also draw attention to the need to reconsider the method of age correction used in the case of PT infants with respect to their language development. Another unresolved question regarding PT infants’ language development is the identification of factors that might explain these infants’ atypical prosodic development.

In this context, our research aimed to investigate word stress processing during the first year of life in PT infants belonging to homogeneous groups according to the clinical exclusion criteria. Our further goals were to (1) reveal whether the PT infants’ long-term native language specific stress representation is as stable as that of FT infants if we examined them at the same maturational ages (2) identify the most plausible explanatory factors behind PT infants’ specific prosodic development; and (3) to investigate whether PT infants’ word stress processing is disrupted or delayed; and (4) to demonstrate the explanatory power of birth weight and gestational age after the neonatal period in terms of language development.

Besides the clinical aspect of my dissertation, we aimed to examine how the stress cue and the emerging lexical status interact in typically developing full-term (FT) infants leaving in monolingual Hungarian language environment. In a given language, prosody (word stress) and the phoneme-relevant aspects of speech (phoneme) may serve different functions in terms of acquisition (Becker et al. 2018). We expected that languages differ in timing of this prosodic-phonemic integration process, depending on the stress pattern of the particular language, being variable (e.g. German) or fixed stress (e.g. Hungarian). Our goal was to identify the time point of processing changes when infants learning a fixed stress language, here Hungarian, can integrate these two types of information. The time point of integration could be a sensitive prognostic marker of the typical language development. Therefore, it can reliably sign atypical language development in an early period.

(4)

4 Hypotheses

The four studies presented in the dissertation test three hypotheses.

1) First we hypothesized that lexical status would be found to have a modulation effect on stress processing (interpreted as integration) between 6 and 10 months of age (see our results related to this hypothesis in Thesis Statements 1 and 2).

2) Our second hypotheses was that, despite the application of age correction in PT infants, their long-term stress representation would be found to be unstable compared to that of FT infants due to the modulating role of the shortened intrauterine prosodic experience (see the results related to this hypothesis in Thesis Statements 3 and 4).

3) According to our third hypotheses, although PT infants’ stress sensitivity is not impaired, mainly their stress processing is disrupted rather than delayed. Additionally we hypothesized that besides gestational age, birth weight is an important maturational factor with respect to early prosodic processing (see the results related to this hypothesis in Thesis Statements 5 and 6).

Method

To answer these questions we conducted three ERP experiments (Study I.-II.-III.), and we summarized in our review article (Study IV.) the relevant national and international electrophysiological, brain imaging and behavioral results regarding our hypotheses.

The designs of the experiments were the same as that used for adults (pseudoword paradigm: Honbolygó & Csépe, 2013; word paradigm: Garami et al. 2017). For the methodological details of the ERP experiments see Figure I.

(5)

5

Figure I. Methodological details of the ERP studies

*c: corrected age

In the ERP experiments, stimuli were presented in a passive oddball paradigm in two conditions: 1) Illegal deviant condition: the pseudo word/word with the legal stress pattern was the standard stimulus, and the pseudo word/word with the illegal stress pattern was the

(6)

6

deviant stimulus; 2) Legal deviant condition: the roles of the stimuli were reversed, the pseudo word/word with the illegal stress pattern became the standard, and the pseudo word/word with the legal stress pattern became the deviant stimulus. The electroencephalogram was recorded from 16 scalp locations: F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, O1, Oz, O2,T3, T4, M1, M2. The reference electrode was at Cz, and the ground was between Fz and Fpz on the midline. We analyzed the mismatch response, the electrophysiological correlate of acoustic change detection.

Thesis Statements

Thesis Statement 1: Lexical status modulates stress pattern discrimination at 6 and 10 months of age in Hungarian-learning infants.

Study I investigated the modulation effect of lexical status on word stress discrimination. By comparing the MMRs elicited by the pseudowords and words, we found different MMRs as a function of lexicality. Due to the suppression effect of lexicality in the illegal deviant condition of the word stimulus, no MMR was obtained in the first time window, which is a typical response pattern in the case of pseudowords. In the second time window in this condition, we found a P-MMR elicited by stress on the second syllable in the words, but not in the pseudowords. In the second time window in the legal deviant condition, we found mismatch negativity responses (N-MMRs) in the case of the words, but not the pseudowords. We interpreted these latter P-MMRs and N-MMRs as being the result of the facilitation effect of lexical status on stress processing as early as 6 months of age.

Publication related to this point:

Ragó A., Varga Zs., Garami L., Honbolygó F, Csépe V. (2021). Effect of lexical status on prosodic processing in infants, learning a fixed stress language. Psychophysiology,00,e1-13.

https://doi.org/10.1111/psyp.13932

(7)

7

Thesis Statement 2: Age differences imply the possible time of integration of lexical and stress cues in Hungarian

In Study I the effect of age was also investigated with respect to the integration process. In the legal deviant condition of the word (first time window), where the lexical and stress cues conflicted, we found an N-MMR in the 6-month-olds only. Their response was similar to that found in the case of the pseudowords. Our interpretation was that, due to the integration of the lexical and stress cues, no N-MMR was obtained in the 10-month-old infants. According to our interpretation, this age difference is attributable to the time of the integration process.

Publication related to this point:

Ragó A., Varga Zs., Garami L., Honbolygó F, Csépe V. (2021). Effect of lexical status on prosodic processing in infants, learning a fixed stress language. Psychophysiology,00,e1-13.

https://doi.org/10.1111/psyp.13932

Thesis Statement 3: Despite the application of age correction, unstable long-term stress representation was found in 6- and 10-month-old PT infants due to the shortened in utero prosodic experience.

In Study II, word-level stress processing in PT and FT infants was examined at 6 and 10 months of corrected age using pseudowords. Legal stress occurring in different roles (standard vs. deviant) elicited a specific ERP pattern in PT infants, but not in FT infants. We interpreted this as revealing that the memory structures for the native stress pattern are unstable in PT infants at these ages and that, due to this instability, the native language deviant is processed at a different level of effort compared to the native language standard. Behind this representational instability several explanatory factors emerge (white matter structural abnormalities, neural immaturity, insufficient extrauterine language experience, less

(8)

8

intrauterine experience). According to the results of longitudinal studies, language disorders cannot be attributed exclusively to white matter abnormalities registered at term-equivalent age, nor can the results be explained by the different maturational level, as the PT infants’

ages were corrected. Age adjustment also raises the question of whether longer extrauterine language experience compared to FT infants is able to facilitate the acquisition of the prosodic properties of the mother tongue in the case of PT infants. The most plausible explanation is that longer extrauterine language experience is not able to compensate for the effect of shortened intrauterine prosodic experience in PT infants. This line of our argument was further strengthened by testing the effect of the severity of prematurity (see Thesis Statement 4).

Publications related to this point:

Varga, Zs., Garami, L., Ragó, A., Honbolygó, F., Csépe, V. (2019). Does intra-uterine language

experience modulate word stress processing? An ERP study. Research in Developmental Disabilities, 90, 59-71. https://doi.org/10.1016/j.ridd.2019.04.011

Varga Zs., Szabó, M. Csépe, V. (2020). Characteristics and risk factors of language development in preterm infants. Hungarian Review of Psychology, 75,2/17, 289-314. DOI: 10.1556/0016.2020.00017

Thesis Statement 4: Less severe prematurity is associated with better stress discrimination.

In Study II, the ERP responses elicited by the pseudowords in very and moderate-to-late PT infants (at 6 and 10 months of corrected age) were compared. The standards and deviants elicited significantly different ERP responses in the group of moderate-to-late PT infants. This response pattern was absent in the group of very PT infants, despite the matched age correction in the two groups. These analyses also revealed that neither longer extrauterine language experience nor age correction for the neural immaturity of the PT infants eliminated

(9)

9

the processing differences compared to the FT infants. The most plausible explanation is that their auditory system had not been tuned to the prosodic properties of the native language in the third trimester due to the shortened intrauterine prosodic experience. Gestational age proved to be a determining perinatal risk factor with respect to prosodic development in the second half of the first year of life.

Varga, Zs., Garami, L., Ragó, A., Honbolygó, F., Csépe, V. (2019). Does intra-uterine language

experience modulate word stress processing? An ERP study. Research in Developmental Disabilities, 90, 59-71. https://doi.org/10.1016/j.ridd.2019.04.011

Thesis Statement 5: In PT infants, stress sensitivity is not impaired. Word stress processing in PT infants seems to be disrupted, not merely delayed.

In Study III, we used the same pseudoword oddball paradigm as in Study II, but we registered the ERP responses at further ages (FT4 vs. PT6; FT10 vs. PT12) in order to investigate the developmental course of stress processing. Our results showed that stress sensitivity is unimpaired in PT infants, as we also found MMRs in the legal and illegal stress pattern discrimination. We also found significant differences between the PT and FT infants (at both tested time points in the first year of life) in terms of MMR amplitudes and polarity.

These results suggest PT infants’ stress processing is not only delayed but is rather disrupted.

Varga, Zs., Ragó, A., Honbolygó, F., Csépe, V. (2021). Disrupted or delayed? Stress discrimination among preterm as compared to full-term infants during the first year of life. Infant Behavior and Development,62,101520. https://doi.org/10.1016/j.infbeh.2020.101520

(10)

10

Thesis Statement 6: The explanatory power of birth weight is greater than that of gestational age with respect to the MMRs elicited by stress pattern discrimination.

In Study III, the explanatory power of gestational age and birth weight were compared in terms of the amplitude of the MMRs. In Study III, birth weight in the PT6 group explained 21% of the total variance of the P-MMRs. However, gestational age had no explanatory power of its own. According to our results, the higher the birth weight, the greater the MMR amplitude will be.

Varga, Zs., Ragó, A., Honbolygó, F., Csépe, V. (2021). Disrupted or delayed? Stress discrimination

among preterm as compared to full-term infants during the first year of life. Infant Behavior and Development,62,101520. https://doi.org/10.1016/j.infbeh.2020.101520

Summary, conclusions

Our main finding is that the integration of prosodic cues and lexical information starts earlier in a fixed stress language than in variable stress languages where word stress also plays a role in the segmentation process and modifies meaning. In order to test the integration process thoroughly, cross-linguistic studies are needed.

The second main finding of the studies described in the present dissertation is that, compared to FT infants, the development of word stress processing in very and moderate-to-

(11)

11

late PT infants seems still to be disrupted in the first year of life. We found that PT infants’

long-term language-specific stress representation is unstable. According to our interpretation, this can be considered a risk factor for subsequent language development in the longer term. It is important to highlight that (1) these PT infants were born without structural brain abnormalities; and (2) their age was adjusted to the expected date of delivery. Our results also indicate that infants who miss out on intrauterine prosodic experience (deaf infants, PT infants) are at risk of atypical language processing. Our results are in line with studies that emphasize the importance of reconsidering the method of age correction with a focus on the language domain.

Based on our results, it is important to emphasize to neurologists and developmental psychologists that PT infants born after 30 weeks of gestation are also at risk of disrupted prosodic processing, which may have consequences in terms of the language acquisition process. In spite of that, this sample of PT infants can be considered as slightly at risk of atypical cognitive development in clinical practice. Our results may affect the prognostic work of clinicians, in the sense that we have revealed that, besides gestational age, birth weight should also be taken into consideration with respect to the development of auditory skills in PT infants. This is also the case in the sample of PT infants whose gestational age was above 30 weeks of gestation, and whose birth weight was appropriate for their gestational age.

Publications cited in the Thesis Booklet

Barre, N., Morgan, A., Doyle, L. W., & Anderson, P. J. (2011). Language Abilities in Children Who Were Very Preterm and/or Very Low Birth Weight: A Meta-Analysis. The Journal of Pediatrics, 158(5), 766–774.e1. https://doi.org/10.1016/j.jpeds.2010.10.032

Bisiacchi, P. S., Mento, G., & Suppiej, A. (2009). Cortical auditory processing in preterm newborns:

An ERP study. Biological Psychology, 82(2), 176–185.

https://doi.org/10.1016/j.biopsycho.2009.07.005

Becker, A., Schild, U., & Friedrich, C. K. (2018). Tracking independence and merging of prosodic and phonemic processing across infancy. Developmental Science, 21, 1–11.

https://doi.org/10.1111/desc.12525

Ference, J., & Curtin, S. (2013). Attention to lexical stress and early vocabulary growth in 5-month-

(12)

12

olds at risk for autism spectrum disorder. Journal of Experimental Child Psychology, 116(4), 891–903. https://doi.org/10.1016/j.jecp.2013.08.006

Friedrich, M., Herold, B., & Friederici, A. D. (2009). ERP correlates of processing native and non- native language word stress in infants with different language outcomes. CORTEX, 45(5), 662–

676. https://doi.org/10.1016/j.cortex.2008.06.014

Garami, L., Ragó, A., Honbolygó, F., & Csépe, V. (2017). Lexical influence on stress processing in a fixed-stress language. International Journal of Psychophysiology, 117, 10–16.

https://doi.org/10.1016/j.ijpsycho.2017.03.006

Gervain, J. (2018). The role of prenatal experience in language development. Current Opinion in Behavioral Sciences, 21, 62–67. https://doi.org/10.1016/j.cobeha.2018.02.004

Honbolygó, F., & Csépe, V. (2013). Saliency or template? ERP evidence for long-term representation of word stress. International Journal of Psychophysiology, 87(2), 165–172.

https://doi.org/10.1016/j.ijpsycho.2012.12.005

Mento, G., Suppiej, A., & Altoe, G. (2010). Functional hemispheric asymmetries in humans :

electrophysiological evidence from preterm infants. European Journal of Neuroscience, 31, 565–

574. https://doi.org/10.1111/j.1460-9568.2010.07076.x

Pena, M., Pittaluga, E., & Mehler, J. (2010). Language acquisition in premature and full-term infants.

Proceedings of the National Academy of Sciences, 107(8), 3823–3828.

https://doi.org/10.1073/pnas.0914326107

Pena, M., Werker, J. F., & Dehaene-lambertz, G. (2012). Earlier Speech Exposure Does Not Accelerate Speech Acquisition. Journal of Neuroscience, 32(33), 11159–11163.

https://doi.org/10.1523/JNEUROSCI.6516-11.2012

Pritchard, V., Bora, S., Austin, N. C., Levin, K. J., & Woodward, L. J. (2014). Identifying Very Preterm Children at Educational Risk Using a School Readiness Framework. Pediatrics, e825–

e832. https://doi.org/10.1542/peds.2013-3865

Ragó, A., Honbolygó, F., Róna, Z., Beke, A., & Csépe, V. (2014). Effect of maturation on

suprasegmental speech processing in full- and preterm infants: A mismatch negativity study.

Research in Developmental Disabilities, 35(1), 192–202.

(13)

13 https://doi.org/10.1016/j.ridd.2013.10.006

Sansavini, A., Guarini, A., Justice, L. M., Savini, S., Broccoli, S., Alessandroni, R., & Faldella, G.

(2010). Does preterm birth increase a childs risk for language impairment ? Early Human Development, 86(12), 765–772. https://doi.org/10.1016/j.earlhumdev.2010.08.014